Accumulation of Stimulants of Toll-Like Receptor (TLR)-2 and TLR4 in Meat Products Stored at 5 °C

:  Recent evidence suggests that exposure to stimulants of the innate immune receptors Toll‐like receptor (TLR)‐2 and TLR4 may contribute to the development of atherosclerosis and insulin resistance. We showed recently that common foodsuffs can contain TLR‐stimulants, and that the greatest concentra...

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Published inJournal of food science Vol. 76; no. 2; pp. H72 - H79
Main Author Erridge, Clett
Format Journal Article
LanguageEnglish
Published Malden, USA Blackwell Publishing Inc 01.03.2011
Wiley
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Abstract :  Recent evidence suggests that exposure to stimulants of the innate immune receptors Toll‐like receptor (TLR)‐2 and TLR4 may contribute to the development of atherosclerosis and insulin resistance. We showed recently that common foodsuffs can contain TLR‐stimulants, and that the greatest concentrations were present in meat‐based products. Using a recently developed quantitative bioassay, we here examined the kinetics of accumulation of TLR2‐ and TLR4‐stimulants in a variety of meat products held at 5 °C in air or under a modified atmosphere for up to 8 d. Meat content of TLR‐stimulants increased with time in each meat examined and was paralleled by growth of pseudomonads and Enterobacteriaceae, suggesting that bacterial lipopeptides and lipopolysaccharides are the likely sources of TLR2‐ and TLR4‐stimulants, respectively. TLR‐stimulants reached the highest levels (approximately 80 μg lipopeptide‐equivalents per gramme and approximately 7 μg lipopolysaccharide‐equivalents per gram) in meat that was minced rather than intact, and when stored in air rather than under a modified atmosphere. TLR2‐ and TLR4‐stimulants in meat products cooked for 1 h retained approximately 20% and approximately 40% of their bioactivity, respectively. In summary, storage conditions and microbial flora critically regulate the kinetics of TLR2‐ and TLR4‐stimulant accumulation in meat products and these may retain biological activity after cooking. Practical Application:  The novel assays presented in this work could be used to predict the potential of foodstuffs to promote inflammatory signaling in human subjects, which may be deleterious to health. These assays may also be used to monitor the historical microbial flora in food products after cooking or other forms of food processing may have rendered the original microflora nonviable.
AbstractList :  Recent evidence suggests that exposure to stimulants of the innate immune receptors Toll‐like receptor (TLR)‐2 and TLR4 may contribute to the development of atherosclerosis and insulin resistance. We showed recently that common foodsuffs can contain TLR‐stimulants, and that the greatest concentrations were present in meat‐based products. Using a recently developed quantitative bioassay, we here examined the kinetics of accumulation of TLR2‐ and TLR4‐stimulants in a variety of meat products held at 5 °C in air or under a modified atmosphere for up to 8 d. Meat content of TLR‐stimulants increased with time in each meat examined and was paralleled by growth of pseudomonads and Enterobacteriaceae, suggesting that bacterial lipopeptides and lipopolysaccharides are the likely sources of TLR2‐ and TLR4‐stimulants, respectively. TLR‐stimulants reached the highest levels (approximately 80 μg lipopeptide‐equivalents per gramme and approximately 7 μg lipopolysaccharide‐equivalents per gram) in meat that was minced rather than intact, and when stored in air rather than under a modified atmosphere. TLR2‐ and TLR4‐stimulants in meat products cooked for 1 h retained approximately 20% and approximately 40% of their bioactivity, respectively. In summary, storage conditions and microbial flora critically regulate the kinetics of TLR2‐ and TLR4‐stimulant accumulation in meat products and these may retain biological activity after cooking. Practical Application:  The novel assays presented in this work could be used to predict the potential of foodstuffs to promote inflammatory signaling in human subjects, which may be deleterious to health. These assays may also be used to monitor the historical microbial flora in food products after cooking or other forms of food processing may have rendered the original microflora nonviable.
Recent evidence suggests that exposure to stimulants of the innate immune receptors Toll-like receptor (TLR)-2 and TLR4 may contribute to the development of atherosclerosis and insulin resistance. We showed recently that common foodsuffs can contain TLR-stimulants, and that the greatest concentrations were present in meat-based products. Using a recently developed quantitative bioassay, we here examined the kinetics of accumulation of TLR2- and TLR4-stimulants in a variety of meat products held at 5 °C in air or under a modified atmosphere for up to 8 d. Meat content of TLR-stimulants increased with time in each meat examined and was paralleled by growth of pseudomonads and Enterobacteriaceae, suggesting that bacterial lipopeptides and lipopolysaccharides are the likely sources of TLR2- and TLR4-stimulants, respectively. TLR-stimulants reached the highest levels (approximately 80 ¨g lipopeptide-equivalents per gramme and approximately 7 ¨g lipopolysaccharide-equivalents per gram) in meat that was minced rather than intact, and when stored in air rather than under a modified atmosphere. TLR2- and TLR4-stimulants in meat products cooked for 1 h retained approximately 20% and approximately 40% of their bioactivity, respectively. In summary, storage conditions and microbial flora critically regulate the kinetics of TLR2- and TLR4-stimulant accumulation in meat products and these may retain biological activity after cooking. [PUBLICATION ABSTRACT]
Recent evidence suggests that exposure to stimulants of the innate immune receptors Toll‐like receptor (TLR)‐2 and TLR4 may contribute to the development of atherosclerosis and insulin resistance. We showed recently that common foodsuffs can contain TLR‐stimulants, and that the greatest concentrations were present in meat‐based products. Using a recently developed quantitative bioassay, we here examined the kinetics of accumulation of TLR2‐ and TLR4‐stimulants in a variety of meat products held at 5 °C in air or under a modified atmosphere for up to 8 d. Meat content of TLR‐stimulants increased with time in each meat examined and was paralleled by growth of pseudomonads and Enterobacteriaceae, suggesting that bacterial lipopeptides and lipopolysaccharides are the likely sources of TLR2‐ and TLR4‐stimulants, respectively. TLR‐stimulants reached the highest levels (approximately 80 μg lipopeptide‐equivalents per gramme and approximately 7 μg lipopolysaccharide‐equivalents per gram) in meat that was minced rather than intact, and when stored in air rather than under a modified atmosphere. TLR2‐ and TLR4‐stimulants in meat products cooked for 1 h retained approximately 20% and approximately 40% of their bioactivity, respectively. In summary, storage conditions and microbial flora critically regulate the kinetics of TLR2‐ and TLR4‐stimulant accumulation in meat products and these may retain biological activity after cooking. Practical Application:  The novel assays presented in this work could be used to predict the potential of foodstuffs to promote inflammatory signaling in human subjects, which may be deleterious to health. These assays may also be used to monitor the historical microbial flora in food products after cooking or other forms of food processing may have rendered the original microflora nonviable.
Recent evidence suggests that exposure to stimulants of the innate immune receptors Toll-like receptor (TLR)-2 and TLR4 may contribute to the development of atherosclerosis and insulin resistance. We showed recently that common foodsuffs can contain TLR-stimulants, and that the greatest concentrations were present in meat-based products. Using a recently developed quantitative bioassay, we here examined the kinetics of accumulation of TLR2- and TLR4-stimulants in a variety of meat products held at 5 °C in air or under a modified atmosphere for up to 8 d. Meat content of TLR-stimulants increased with time in each meat examined and was paralleled by growth of pseudomonads and Enterobacteriaceae, suggesting that bacterial lipopeptides and lipopolysaccharides are the likely sources of TLR2- and TLR4-stimulants, respectively. TLR-stimulants reached the highest levels (approximately 80 μg lipopeptide-equivalents per gramme and approximately 7 μg lipopolysaccharide-equivalents per gram) in meat that was minced rather than intact, and when stored in air rather than under a modified atmosphere. TLR2- and TLR4-stimulants in meat products cooked for 1 h retained approximately 20% and approximately 40% of their bioactivity, respectively. In summary, storage conditions and microbial flora critically regulate the kinetics of TLR2- and TLR4-stimulant accumulation in meat products and these may retain biological activity after cooking. The novel assays presented in this work could be used to predict the potential of foodstuffs to promote inflammatory signaling in human subjects, which may be deleterious to health. These assays may also be used to monitor the historical microbial flora in food products after cooking or other forms of food processing may have rendered the original microflora nonviable.
Recent evidence suggests that exposure to stimulants of the innate immune receptors Toll-like receptor (TLR)-2 and TLR4 may contribute to the development of atherosclerosis and insulin resistance. We showed recently that common foodsuffs can contain TLR-stimulants, and that the greatest concentrations were present in meat-based products. Using a recently developed quantitative bioassay, we here examined the kinetics of accumulation of TLR2- and TLR4-stimulants in a variety of meat products held at 5 °C in air or under a modified atmosphere for up to 8 d. Meat content of TLR-stimulants increased with time in each meat examined and was paralleled by growth of pseudomonads and Enterobacteriaceae, suggesting that bacterial lipopeptides and lipopolysaccharides are the likely sources of TLR2- and TLR4-stimulants, respectively. TLR-stimulants reached the highest levels (approximately 80 μg lipopeptide-equivalents per gramme and approximately 7 μg lipopolysaccharide-equivalents per gram) in meat that was minced rather than intact, and when stored in air rather than under a modified atmosphere. TLR2- and TLR4-stimulants in meat products cooked for 1 h retained approximately 20% and approximately 40% of their bioactivity, respectively. In summary, storage conditions and microbial flora critically regulate the kinetics of TLR2- and TLR4-stimulant accumulation in meat products and these may retain biological activity after cooking.UNLABELLEDRecent evidence suggests that exposure to stimulants of the innate immune receptors Toll-like receptor (TLR)-2 and TLR4 may contribute to the development of atherosclerosis and insulin resistance. We showed recently that common foodsuffs can contain TLR-stimulants, and that the greatest concentrations were present in meat-based products. Using a recently developed quantitative bioassay, we here examined the kinetics of accumulation of TLR2- and TLR4-stimulants in a variety of meat products held at 5 °C in air or under a modified atmosphere for up to 8 d. Meat content of TLR-stimulants increased with time in each meat examined and was paralleled by growth of pseudomonads and Enterobacteriaceae, suggesting that bacterial lipopeptides and lipopolysaccharides are the likely sources of TLR2- and TLR4-stimulants, respectively. TLR-stimulants reached the highest levels (approximately 80 μg lipopeptide-equivalents per gramme and approximately 7 μg lipopolysaccharide-equivalents per gram) in meat that was minced rather than intact, and when stored in air rather than under a modified atmosphere. TLR2- and TLR4-stimulants in meat products cooked for 1 h retained approximately 20% and approximately 40% of their bioactivity, respectively. In summary, storage conditions and microbial flora critically regulate the kinetics of TLR2- and TLR4-stimulant accumulation in meat products and these may retain biological activity after cooking.The novel assays presented in this work could be used to predict the potential of foodstuffs to promote inflammatory signaling in human subjects, which may be deleterious to health. These assays may also be used to monitor the historical microbial flora in food products after cooking or other forms of food processing may have rendered the original microflora nonviable.PRACTICAL APPLICATIONThe novel assays presented in this work could be used to predict the potential of foodstuffs to promote inflammatory signaling in human subjects, which may be deleterious to health. These assays may also be used to monitor the historical microbial flora in food products after cooking or other forms of food processing may have rendered the original microflora nonviable.
Author Erridge, Clett
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  surname: Erridge
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  email: Author Erridge is with Dept. of Cardiovascular Sciences, Glenfield General Hospital, Univ. of Leicester, Groby Road, Leicester, LE3 9QP, U.K. Direct inquiries to author Erridge ( ce55@le.ac.uk).
  organization: Author Erridge is with Dept. of Cardiovascular Sciences, Glenfield General Hospital, Univ. of Leicester, Groby Road, Leicester, LE3 9QP, U.K. Direct inquiries to author Erridge (E-mail: ce55@le.ac.uk)
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Keywords Lipopolysaccharide
Meat product
Toll-like receptors
Bacteria
Inflammation
Lipopeptide
Meat
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Yoshino S, Sasatomi E, Mori Y, Sagai M. 1999. Oral administration of lipopolysaccharide exacerbates collagen-induced arthritis in mice. J Immunol 163:3417-22.
Jay JM, Vilai JP, Hughes ME. 2003. Profile and activity of the bacterial biota of ground beef held from freshness to spoilage at 5-7 degrees C. Int J Food Microbiol 81:105-11.
Erridge C. 2009. The roles of Toll-like receptors in atherosclerosis. J Innate Immun 1:340-9.
Ghoshal S, Witta J, Zhong J, de Villiers W, Eckhardt E. 2009. Chylomicrons promote intestinal absorption of lipopolysaccharides. J Lipid Res 50:90-7.
Robinson RT, Khader SA, Locksley RM, Lien E, Smiley ST, Cooper AM. 2008. Yersinia pestis evades TLR4-dependent induction of IL-12(p40)2 by dendritic cells and subsequent cell migration. J Immunol 181:5560-7.
Mullick AE, Tobias PS, Curtiss LK. 2005. Modulation of atherosclerosis in mice by Toll-like receptor 2. J Clin Invest 115:3149-56.
Krogh-Madsen R, Plomgaard P, Akerstrom T, Møller K, Schmitz O, Pedersen BK. 2008. Effect of short-term intralipid infusion on the immune response during low-dose endotoxemia in humans. Am J Physiol Endocrinol Metab 294:E371-9.
Westerterp M, Berbée JF, Pires NM, van Mierlo GJ, Kleemann R, Romijn JA, Havekes LM, Rensen PC. 2007. Apolipoprotein C-I is crucially involved in lipopolysaccharide-induced atherosclerosis development in apolipoprotein E-knockout mice. Circulation 116:2173-81.
Madan M, Amar S. 2008. Toll-like receptor-2 mediates diet and/or pathogen associated atherosclerosis: proteomic findings. PLoS ONE 3:e3204.
Hajjar AM, Ernst RK, Tsai JH, Wilson CB, Miller SI. Human toll-like receptor 4 recognises host-specific LPS modifications. Nat Immunol 3:354-9 (2003)
Wiedermann CI, Kiechl S, Dunzendorfer S, Schratzberger P, Egger G, Oberhollenzer F, Willeit J. 1999.Association of endotoxaemia with carotid atherosclerosis and cardiovascular disease: prospective results from the Bruneck Study. J Am Coll Cardiol 34:1975-81.
Borch E, Kant-Muermans ML, Blixt Y. 1996. Bacterial spoilage of meat and cured meat products. Int J Food Microbiol 33:103-20.
Erridge C, Duncan SH, Bereswill S, Heimesaat MM. 2010. The induction of colitis and ileitis in mice is associated with marked increases in intestinal concentrations of stimulants of TLRs 2, 4, and 5. PLoS ONE 5:e9125.
Fallowfield HJ, Patterson JT. 1985. Potential value of the Limulus lysate assay for the measurement of meat spoilage. Int J Food Sci Tech 20:467-79.
Lambropoulou KA, Drosinos EH, Nychas GJ. 1996. The effect of glucose supplementation on the spoilage microflora and chemical composition of minced beef stored aerobically or under a modified atmosphere at 4 degrees C. Int J Food Microbiol 30:281-91.
Jay JM, Margitic S, Shereda AL, Covington HV. 1979. Determining endotoxin content of ground beef by the Limulus amoebocyte lysate test as a rapid indicator of microbial quality. Appl Environ Microbiol 38:885-90.
Ross R. 1999. Atherosclerosis is an inflammatory disease. Am Heart J 138:S419-20.
Al-Attas OS, Al-Daghri NM, Al-Rubeaan KA, da Silva NF, Sabico SL, Kumar S, McTernan PG, Harte AL. 2009. Changes in endotoxin levels in T2DM subjects on anti-diabetic therapies. Cardiovasc Diabetol 8:20.
Erridge C. 2010. The capacity of foodstuffs to induce innate immune activation of human monocytes in vitro is dependent on food content of stimulants of Toll-like receptors 2 and 4. Br J Nutr 20:1-9.
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Gram L, Ravn L, Rasch M, Bruhn JB, Christensen AB, Givskov M. 2002. Food spoilage - interactions between food spoilage bacteria. Int J Food Microbiol 78:79-97.
Tsukumo DM, Carvalho-Filho MA, Carvalheira JB, Prada PO, Hirabara SM, Schenka AA, Araújo EP, Vassallo J, Curi R, Velloso LA, Saad MJ. 2007. Loss-of-function mutation in Toll-like receptor 4 prevents diet-induced obesity and insulin resistance. Diabetes 56:1986-98.
Elin R, Wolff S. 1973. Nonspecificity of the Limulus amebocyte lysate test: positive reactions with polynucleotides and proteins. J Infect Dis 128:349-52.
Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ, Sole J, Nichols A, Ross JS, Tartaglia LA, Chen H. 2003. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112:1821-30.
Erridge C, Burdess A, Jackson AJ, Murray C, Riggio M, Lappin D, Milligan S, Spickett CM, Webb DJ. 2008. Vascular cell responsiveness to Toll-like receptor ligands in carotid atheroma. Eur J Clin Invest 38:713-20.
Mehta NN, McGillicuddy FC, Anderson PD, Hinkle CC, Shah R, Pruscino L, Tabita-Martinez J, Sellers KF, Rickels MR, Reilly MP. 2010. Experimental endotoxemia induces adipose inflammation and insulin resistance in humans. Diabetes 59:172-81.
Creely SJ, McTernan PG, Kusminski CM, Fisher M, Khanolkar M, Evans M, Harte AL, Kumar S. 2007. Lipopolysaccharide activates an innate immune system response in human adipose tissue in obesity and type 2 diabetes. Am J Physiol Endocrinol Metab 292:E740-7.
Rossignol D, Lynn M, Wittek A, Rose J, Solomon S, Natanson C, Eichacker P. 2006. Elevated plasma levels of limulus amoebocyte lysate- reactive material. Authors' reply. J Infect Dis 194:1340-1.
2004; 101
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Snippet :  Recent evidence suggests that exposure to stimulants of the innate immune receptors Toll‐like receptor (TLR)‐2 and TLR4 may contribute to the development of...
Recent evidence suggests that exposure to stimulants of the innate immune receptors Toll‐like receptor (TLR)‐2 and TLR4 may contribute to the development of...
Recent evidence suggests that exposure to stimulants of the innate immune receptors Toll-like receptor (TLR)-2 and TLR4 may contribute to the development of...
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StartPage H72
SubjectTerms Accumulation
Animals
Atherosclerosis
Atmosphere
Bacteria
Bioassays
Biological and medical sciences
Biological Assay - methods
Cattle
Cold Temperature
Enterobacteriaceae - growth & development
Flora
Food Handling
Food industries
Food Preservation - methods
Fundamental and applied biological sciences. Psychology
inflammation
Inflammation - metabolism
Inflammation - pathology
Insulin resistance
Kinetics
lipopeptide
Lipopeptides - metabolism
lipopolysaccharide
Lipopolysaccharides - metabolism
Meat
Meat and meat product industries
Meat Products
Peptides
Pseudomonas - growth & development
Stimulants
Swine
T cell receptors
Toll-Like Receptor 2 - metabolism
Toll-Like Receptor 4 - metabolism
Toll-like receptors
Turkeys
Title Accumulation of Stimulants of Toll-Like Receptor (TLR)-2 and TLR4 in Meat Products Stored at 5 °C
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https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fj.1750-3841.2010.02018.x
https://www.ncbi.nlm.nih.gov/pubmed/21535770
https://www.proquest.com/docview/864650595
https://www.proquest.com/docview/864787537
Volume 76
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